Hormones – International Journal of Endocrinology and Metabolism

Evaluation of the possible impact of the fear of hypoglycaemia on diabetes

management in children and adolescents with type 1 Diabetes Mellitus and their
parents - A cross-sectional study.
--Manuscript Draft--

Manuscript Number:

Full Title: Evaluation of the possible impact of the fear of hypoglycaemia on diabetes
management in children and adolescents with type 1 Diabetes Mellitus and their
parents - A cross-sectional study.

Article Type: Original Article

Funding Information:

Abstract: Purpose: Hypoglycaemia represents a significant source of anxiety for children with
type 1 Diabetes Mellitus (T1DM) and their caretakers. Fear of hypoglycaemia (FoH)
was measured in children and adolescents with T1DM as well as in their parents, using
an established research instrument, the Hypoglycaemia Fear Survey (HFS). Methods:
This is a two-centre cross-sectional study involving 100 children and adolescents aged
6-18 years old, diagnosed with T1DM. One parent of each child also participated in the
study. The participants, who were recruited from two different Paediatric Endocrine
Outpatient Clinics, were asked to complete the translated Greek version of the HFS,
which includes one version for children (C-HFS) and one for parents (P-HFS). The
association of the questionnaire responses with subjects’ characteristics, such as
current age, age at diagnosis, duration of diabetes, HbA1c levels and mode of diabetes
treatment and were assessed. Results: Parents exhibited significantly higher mean
HFS scores than their children. No significant correlation was found between the P-
HFS or the C-HFS scores and the age of children, duration of diabetes, HbA1c or
mode of treatment. Conclusion: The finding that parents experience increased levels of
FoH compared to their children emphasizes the importance of healthcare providers
screening for parental FoH and focusing on approaches to support them, in order to
reduce their psychological burden and thus optimize children’s diabetes management.
Keywords: Fear of hypoglycaemia, type 1 diabetes mellitus, hypoglycaemia fear
survey, reliability.

Corresponding Author: OURANIA ANDREOPOULOU

University of Patras Faculty of Medicine: Panepistemio Patron Tmema Iatrikes
GREECE

Corresponding Author Secondary

Information:

Corresponding Author's Institution: University of Patras Faculty of Medicine: Panepistemio Patron Tmema Iatrikes

Corresponding Author's Secondary

Institution:

First Author: OURANIA ANDREOPOULOU

First Author Secondary Information:

Order of Authors: OURANIA ANDREOPOULOU

Eirini Kostopoulou

Eleni Kotanidou

Sophia Daskalaki

Angeliki Vakka

Assimina Galli-Tsinopoulou

Bessie E Spiliotis

Order of Authors Secondary Information:

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Evaluation of the possible impact of the fear of hypoglycaemia on diabetes

1
2 management in children and adolescents with type 1 Diabetes Mellitus and their
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5 parents - A cross-sectional study.
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Ourania Andreopoulou1*, Eirini Kostopoulou2*, Eleni Kotanidou3, Sophia Daskalaki4,
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11 Angeliki Vakka1, Assimina Galli-Tsinopoulou3, Bessie E Spiliotis2
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15 *equal contribution
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17 1. Department of Psychiatry, University of Patras Medical School, Rio, 26500, Greece
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2. Division of Paediatric Endocrinology and Diabetes, Department of Paediatrics,
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22 University of Patras School of Medicine, Patras, 26500, Greece
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24 3. Unit of Paediatric and Adolescent Diabetes Mellitus, Second Department of
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27 Paediatrics, School of Medicine, Faculty of Health Sciences, Aristotle University of
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29 Thessaloniki, AHEPA University Hospital, Thessaloniki, Greece
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32 4. Department of Electrical and Computer Engineering, School of Engineering,
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34 University of Patras, Patras, 26500, Greece
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40 Corresponding author:
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43 Ourania Andreopoulou
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 Abstract
1
2 Purpose: Hypoglycaemia represents a significant source of anxiety for children with
3
4
5 type 1 Diabetes Mellitus (T1DM) and their caretakers. Fear of hypoglycaemia (FoH)
6
7 was measured in children and adolescents with T1DM as well as in their parents, using
8
9
10 an established research instrument, the Hypoglycaemia Fear Survey (HFS). Methods:
11
12 This is a two-centre cross-sectional study involving 100 children and adolescents aged
13
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15 6-18 years old, diagnosed with T1DM. One parent of each child also participated in the
16
17 study. The participants, who were recruited from two different Paediatric Endocrine
18
19
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Outpatient Clinics, were asked to complete the translated Greek version of the HFS,
21
22 which includes one version for children (C-HFS) and one for parents (P-HFS). The
23
24 association of the questionnaire responses with subjects’ characteristics, such as current
25
26
27 age, age at diagnosis, duration of diabetes, HbA1c levels and mode of diabetes
28
29 treatment and were assessed. Results: Parents exhibited significantly higher mean HFS
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32 scores than their children. No significant correlation was found between the P-HFS or
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34 the C-HFS scores and the age of children, duration of diabetes, HbA1c or mode of
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treatment. Conclusion: The finding that parents experience increased levels of FoH
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39 compared to their children emphasizes the importance of healthcare providers screening
40
41 for parental FoH and focusing on approaches to support them, in order to reduce their
42
43
44 psychological burden and thus optimize children’s diabetes management.
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Keywords: Fear of hypoglycaemia, type 1 diabetes mellitus, hypoglycaemia fear
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50 survey, reliability.
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 Introduction
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2 Hypoglycaemia represents the commonest acute complication of type 1 Diabetes
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5 Mellitus (T1DM) [1]. Aggressive HbA1c goals may increase the frequency of
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7 hypoglycaemia, which represents a major limiting factor in the glycaemic control of
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10 T1DM [2]. Due to its high frequency and unpredictability, hypoglycaemia is a
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12 significant source of anxiety for patients with the disease and their caretakers.
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16 Fear of hypoglycaemia (FoH) is a specific fear evoked by the risk and/or occurrence of
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18 hypoglycaemia [3] and is associated with the frequency of severe hypoglycaemic
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21 episodes [4], particularly during the past 3 months [3]. While to some degree this fear
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23 is adaptive, it may disrupt daily activities, such as sleep and exercise. It can also impair
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26 optimal diabetes management and quality of life through obsessive self-monitoring,
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28 dependence on others, frustration, and behaviour that tends to keep blood glucose levels
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30
high [5-8]. FoH has been recorded in family members of both paediatric and adult
31
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33 patients with T1DM and, as expected, more distressing past experiences of
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35 hypoglycaemia, which involved either loss of consciousness or any hypoglycaemic-
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38 related traumatic event, are often associated with higher levels of fear [6, 9, 10].
39
40 Furthermore, research suggests that higher age, the female gender and longer duration
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43 of T1DM could lead young patients and their families to exhibit higher levels of FoH
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45 [11]. According to a study by Patton et al, the commonest reported parental fear
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concerning hypoglycaemia involved episodes during the night and the next most
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50 common fear involved episodes when the child is not supervised by the parents [12].
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54 FoH in children and their parents can be evaluated by the Hypoglycaemia Fear Survey-
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56 II (HFS-II), a widely used research instrument translated into many languages, that has
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demonstrated reliability and validity [13]. Our team has recently translated the HFS
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 into the Greek language and has confirmed its usefulness as a reliable and valid research
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2 tool for assessing the fear of hypoglycaemia in Greek children and adolescents with
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5 T1DM and their parents [14].
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The aim of the current study was to evaluate the association between self-reported FoH
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11 in children and adolescents with T1DM or their parents and demographic or disease-
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13 related factors, including the child’s age, duration of T1DM, recent HbA1c, mode of
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16 treatment and frequency of hypoglycaemic episodes. Furthermore, this is the first study,
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18 to our knowledge, carried out in Greece addressing this crucial component of the
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21 possible impact of FoH on diabetes management.
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24 Materials and methods
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27 Demographics
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29 This is a cross-sectional study conducted between January 2019 and July 2020 in a
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32 sample of 100 Greek children and adolescents, aged 6 to 18 years old, diagnosed with
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34 Type 1 Diabetes Mellitus (T1DM) at least 3 months before the initiation of the study.
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37 Fifty-four of the participants were male. Participants were recruited from two different
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39 centres where they were being actively followed-up: (1) the Outpatient Clinics of the
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41 Division of Paediatric Endocrinology and Diabetes of the University General Hospital
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44 of Patras in Southern Greece and (2) the Outpatient Clinics of the Unit of Paediatric
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46 and Adolescent Diabetes, 2nd Department of Paediatrics, AHEPA General Hospital of
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49 Thessaloniki, in Northern Greece. The duration of diabetes varied from 3 months to
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51 16.73 years (mean ± sd: 5.05 ± 4.09). One parent involved with the participants’
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54 diabetes care also participated. All the participants could read and write in Greek and
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56 had the mental ability to complete the questionnaires. Exclusionary criteria included
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significant comorbidity in the adolescents that could affect psychosocial status, quality
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 of life, or FoH (e.g., cystic fibrosis) and cognitive or learning disabilities in the child or
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2 the parent (e.g., inability to read) that would preclude their ability to complete the study
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5 protocol.
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10 Questionnaires
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12 All the participants were asked to complete the translated Greek language version of
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15 the Hypoglycaemia Fear Survey (HFS), which is the most well-established instrument
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17 assessing FoH [15].
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22 Scale Translation
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24 Permission for this study was obtained from Dr. Linda Gonder-Frederick, the original
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27 co-author and co-creator of the scale, through personal communication via email. Two
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29 forward translations were produced from the original language (source language) to the
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32 target language. Bilingual translators (EK & OA), whose mother tongue is the target
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34 language, produced the two independent translations. The two translators had different
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academic profiles and each produced a written report. The translations were then
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39 compared and discrepancies between them were resolved through interactive
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41 discussions between the translators. This last step converged to a single translation.
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44 Finally, a third translator, BES, who is an expert in the field, native English speaker, and
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46 blind to the original English version, back translated the instrument to its original
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49 language to check validity by ensuring that the translation reflects the same item content
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51 as the original version. Source and back-translated questionnaires were checked for all
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54 such equivalences. Consensus was reached on the items and the final translation was
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56 reviewed and approved by Dr L. Gonder-Frederick.
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 Two versions of the HFS were used, one for children with T1DM (C-HFS) and one for
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2 their parents (P-HFS). The parent version (P-HFS) is a 26-item questionnaire used to
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5 measure parents’ FoH [16]. It is comprised of two subscales, the Behaviour Subscale
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7 and the Worry subscale. The Behaviour Subscale includes 11 items describing diabetes
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10 self-management behaviours aimed at avoiding hypoglycaemia and its negative
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12 consequences (e.g., keeping blood glucose (BG) higher when the adolescent will be
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15 alone). The Worry subscale includes 15 items describing different anxiety-provoking
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17 aspects of hypoglycaemia (e.g., not having food or drink available for treatment). P-
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HFS items are rated on a 5-point Likert scale, ranging from 1 (never) to 5 (always). A
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22 Total HFS score is obtained by adding the Behaviour and Worry subscale items. The
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24 P-HFS also includes the additional Hypoglycaemia History Questionnaire (Part–II)
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27 regarding the frequency of hypoglycaemic episodes of the child over the past 1, 6 or 12
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29 months, while the parent was absent. The child version of HFS (C-HFS) is a 25-item
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32 self-report measure of children’s FoH. The C-HFS is similar to the P-HFS and
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34 comprises a 10-item Behaviour subscale and a 15-item Worry subscale that are scored
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on the same 5-point Likert scale as the P-HFS [16].
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40 Procedure
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43 In addition to their responses to the HFS questionnaire, demographic and disease-
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45 specific data, such as the current age of the participants, the most recent HbA1c and the
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duration of diabetes were also recorded for all participants in the study. The participants
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50 were approached by the Paediatric Endocrine Divisions’ physicians during their visit
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52 to the hospital. HbA1c was measured on the same day with the completion of the HFS
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55 questionnaire for the majority of the children and within 3 weeks from the completion
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57 of the questionnaire for a small minority. The mode of treatment, i.e. Multiple Dose
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60 Insulin Injection Therapy (MDI) or insulin administration via an insulin pump, was also
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 recorded. Parents and children were also asked to fill in a medical history form and
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2 report the number of severe, medium or mild hypoglycaemic episodes children
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5 experienced during the previous year, past semester or past month, respectively. Mild
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7 hypoglycaemia (MiH) was defined as BG < 70 mg/dl, which did not impair the ability
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10 to function. Medium hypoglycaemia (MeH) was defined as BG so low that it interfered
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12 with the child’s ability to function, but the child did not become so mentally disoriented
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15 that self-treatment was not possible. Severe hypoglycaemia (SH) was defined as BG
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17 resulting in neuroglycopenia that interfered with the child’s ability to self-treat due to
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mental disorientation, unconsciousness, or seizures. Lastly, the levels of FoH between
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22 younger (6-12 years old) and older children (>12 years old) and between children with
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24 optimum glycaemic control (HbA1c<7.5%) and those with poor glycaemic control
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27 (HbA1c>7.5%) were compared.
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32 The study was approved by the Research Ethics Committee of the University Hospital
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34 of Patras (IRB number: 348/9.5.2017) and is in full accordance with the Declaration of
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Helsinki of 1975, as revised in 2013. Written informed consent was obtained from the
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39 parents and informed assent from the participating children and adolescents.
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45 Results
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The summarized characteristics of all participants, including current age, age at onset
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50 of T1DM, duration of T1DM and recent measurement of HbA1c, are shown in Table
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52 1. The sample was balanced between genders.
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56 Judging from their mean scores in the HFS, the parents scored higher than the children
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in most items (Figure 1). Q1 (I eat large bedtime snacks), Q6 (I decrease my insulin
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 dose whenever I think that my blood sugar is very low) and Q9 (I restrict my activity
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2 whenever I think that I may have low blood sugar) were the only items where the
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5 children’s mean score was higher than the corresponding mean score of their parents.
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7 In totality, the mean scores for parents were significantly higher for both subscales and
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10 the Total scale (paired T-test, p<0.0005) compared to the children’s corresponding
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12 scores (Table 2).
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16 The analysis of the current study was performed using the mean scores for all subscales
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18 or Total scales, instead of the total scores. This made easier the handling of all missing
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21 values. Eighty-four out of 100 parents responded to all items, 12 missed one item, 3
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23 missed 2 or 3 items and only one missed 6 items from the Behaviour subscale. For the
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26 children the missing values were fewer, i.e. 89 out of 100 responded to all 25 items, 10
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28 missed one item either from the Behaviour or Worry subscale and only one missed 2
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30 items from the Worry subscale.
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34 Correlations between P-HFS/C-HFS scores and patient characteristics
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HFS scores and children’s current age
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39 No significant correlation was observed between the P-HFS scores, both the two
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41 subscales and the Total scale, and the current age of the child (r=0.023, p=0.820; r=-
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44 0.075, p=0.455; r=-0.057, p=0.575; for Behaviour, Worry and Total scale,
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46 respectively). Similarly, there was no significant correlation between the C-HFS scores
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49 (both the two subscales and the Total scale) and the age of the child (r=-0.065, p=0.521;
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51 r=-0.076, p=0.451; r=-0.093, p= 0.358; for Behaviour, Worry and Total scale,
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54 respectively).
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HFS scores and duration of diabetes
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 No significant correlation was found between the P-HFS scores, both the two subscales
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2 and the Total scale, and duration of diabetes (r=0.01, p=0.920; r=-0.112, p= 0.266; r=-
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5 0.089, p=0.378; for Behaviour, Worry and Total scale, respectively). Similarly, there
6
7 was no significant correlation between the C-HFS scores (both the two subscales and
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10 the Total scale) and the duration of diabetes (r=-0.153, p=0.130; r=-0.034, p=0.740; r=-
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12 0.110, p=0.276; for Behaviour, Worry and Total scale, respectively).
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17 HFS scores and recent HbA1c measurement
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There was no significant correlation between the P-HFS scores (both the two subscales
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22 and the Total scale) and children’s HbA1c levels at the time of completion of the
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24 questionnaire (r=0.149, p=0.140; r=0.145, p=0.150; r=0.181, p=0.071; for Behaviour,
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27 Worry and Total scale, respectively). There was also no significant correlation between
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29 the C-HFS scores (both the two subscales and the Total scale) and children’s HbA1c
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32 levels at the time of completion of the questionnaire (r=-0.177, p=0.079; r=0.041,
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34 p=0.687; r=-0.070, p=0.488; for Behaviour, Worry and Total scale, respectively).
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39 Comparisons of the HFS scores in different subgroups
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41 HFS scores in younger versus older children (current age)
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44 The parents of younger children scored on average slightly higher than the parents of
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46 adolescents, however this difference was not significant for any of the subscales or the
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49 Total scale (Table 4). According to the independent samples T-test there was no
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51 significant difference between the two age groups [t(98)=0.457, p=0.649; t(98)=0.711,
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54 p=0.479; t(98)=0.758, p=0.450].
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 Children’s scores were significantly lower than those of their parents, yet there was no
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2 significant difference between the two age groups (Table 3). The results from the
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5 corresponding independent samples T-test were: [t(68)=1.095, p=0.277; t(98)=-0.045,
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7 p=0.964; t(98)=0.506, p=0.614].
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10
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12 HFS scores and mode of treatment (MDI versus insulin pump)
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15 All mean P-HFS scores were slightly, but not significantly, higher for parents of
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17 children treated via an insulin pump compared to those of children who are on MDI
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(Table 3). The results of the independent samples T-test [t(97)=-0.861, p=0.391; t(97)=-
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22 0.158, p=0.875; t(97)=-0.406, p=0.686] demonstrated no significant difference among
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24 the two groups of parents.
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27
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29 Also, the mean C-HFS scores showed no statistical difference between the two groups.
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32 Based on the independent samples T-test, no significant difference was found for any
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34 of the subscales or for the Total scale [t(98)=0.341, p=0.734; t(98)=-0.824, p=0.412;
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t(98)=-0.422, p=0.674].
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41 HFS scores and HbA1c (HbA1c < 7.5% versus HbA1c ≥ 7.5%)
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44 The average HFS scores for the parents of children with recent measurement of HbA1c
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46 > 7.5% were greater than the corresponding average scores of those of children with
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49 recent HbA1c measurement ≤ 7.5% (Table 3). For the parents, the difference was
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51 significant (level of significance: 0.05) only for the Worry subscale and the Total scale
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54 according to a right-sided independent samples T-test and not for the Behaviour
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56 subscale for which the difference was strongly non-significant [t(98)=-0.851, p=0.199;
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t(98)=-2.235, p=0.014; t(98)=-2.281, p=0.013]. For the children, no significant
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 difference was found in the mean scores between the two groups. Also, according to
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2 the independent samples T-tests (two-sided or one-sided) there was no significant
3
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5 difference between the two groups [t(98)=1.857, p=0.066; t(98)=-0.506, p=0.614;
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7 t(98)=0.663, p=0.509].
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9
10
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12 Effect of Hypoglycaemias on HFS scores
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15 Supplementary file 1 summarizes the children’s and parents’ responses regarding the
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17 frequency of severe, moderate and mild hypoglycaemic episodes during the previous
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19
year, previous 6 months and previous month, respectively.
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21
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23 The mean HFS scores of children and parents grouped according to the number of
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26 severe hypoglycaemic episodes (≤1 versus >1) over the previous one year, moderate
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28 episodes (≤2 versus >2) over the previous 6 months and mild episodes (≤3 versus >3)
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30 over the previous 1 month, are shown in (Table 4).
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32
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34 With regard to severe hypoglycaemic episodes and according to the independent
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37
samples T-test there was no significant difference between the mean scores of the
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39 parents of the two groups of children [t(93)=0.81, p=0.935; t(93)=0.764, p=0.447;
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41 t(93)=0.700, p=0.486; for Behaviour, Worry and Total scale, respectively]. The average
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44 scores of children with more than one SH episode during the last year were consistently
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46 lower than the corresponding average scores of those with none or one SH episode.
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49 According to the independent samples T-test, however, the difference was significant
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51 only for the Behaviour scale and the Total HFS scale [t(89)=3.66, p<0.0005;
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54 t(89)=2.50, p=0.014] but not for the Worry subscale [t(89)=0.766, p=0.446].
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 Similarly, regarding the moderate hypoglycaemic episodes that occurred during the
1
2 previous 6 months, according to the independent samples T-test there was no significant
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4
5 difference between the mean HFS scores for the parents of the two groups of children
6
7 for either subscale or the Total scale [t(84)=1.278, p=0.205; t(56)=-0.325, p=0.747;
8
9
10 t(57)=0.045, p=0.964]. In contrast, the children who had ≤2 MeH exhibited consistently
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12 higher average scores compared to those who had >2 MeH. According to the
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15 independent samples T-test, there was a significant difference between the two groups
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17 of children for the Behaviour subscale and the Total HFS scale [t(89)=3.22, p=0.002;
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19
t(89)=2.62, p=0.01], but not for the Worry subscale [t(89)=1.20, p=0.234].
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21
22
23
24 Lastly, with respect to MiH during the previous one month, according to the
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27 independent samples T-test there was no significant difference between the scores of
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29 any of the HFS subscales or the Total scale for the parents of the two groups of children
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31
32 [t(94)=-1.651, p<0.102; t(94)=-1.816, p=0.073; t(94)=-2.074, p=0.041, respectively],
33
34 as well as for the children [t(90)=-0.60, p<0.549; t(90)=0.547, p=0.586; t(90)=0.069,
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37
p=0.945, respectively].
38
39
40 Discussion
41
42
43 Maintenance of good glycaemic control and prevention of late microvascular and
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45 macrovascular diabetes complications, while avoiding episodes of hypoglycaemia,
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48
represent a challenge in the management of T1DM. However, it is not only the
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50 uncomfortable and embarrassing nature of the symptoms that makes hypoglycaemias a
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52 stressful experience, but predominantly the life-threatening nature of the condition. As
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55 a result, fear of hypoglycaemia evoked by the risk and/or occurrence of low blood
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57 glucose levels, appears to be a common psychosocial consequence among patients
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60 with T1DM [18]. A certain level of fear is beneficial and helps maintain optimum
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 glycaemic control, but extreme fear may impair the person’s well-being, self-
1
2 management, health, and quality of life. Different counteractive strategies may be
3
4
5 used by children with T1DM or their parents in order to avoid hypoglycaemias due to
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7 their fear, including increased intake of carbohydrates, avoidance of physical activity
8
9
10 and administering less insulin than required [19-21]. In this case scenario, the question
11
12 of potential endangerment of optimal glucose management is raised. Interestingly
13
14
15 though, despite aiming at keeping the blood glucose concentrations at higher levels, a
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17 clear association between FoH and HbA1c has not been confirmed [16, 22, 23].
18
19
20
21 In the present study we attempted to evaluate the FoH in Greek children and adolescents
22
23 with T1DM and their parents by using the validated Greek version of the HFS
24
25
26 questionnaire. One of the most important findings of the current study was the
27
28 increased FoH documented in the parents of children with T1DM compared to their
29
30 children. This finding may be of clinical relevance since, according to the literature,
31
32
33 fearful parents may intentionally keep their children’s BG high in an effort to prevent
34
35 hypoglycaemia [8]. However, other studies have not found an association between
36
37
38 parental FoH and suboptimal glycaemic control in paediatric patients [24]. Similarly,
39
40 in the present study the FoH in the parents and the children was not highly correlated
41
42
43 with the HbA1c. Interestingly, though, parental FoH was significantly higher in the
44
45 case of children with HbA1c of above 7.5% and this involved only the Worry subscale
46
47
48
and the Total scale of HFS. It is reasonable to hypothesize that increased parental fear
49
50 of hypoglycaemia may account for greater impaired glucose regulation as expressed by
51
52 HbA1c levels of above 7.5%, although causality cannot be established. In contrast, no
53
54
55 difference was documented in the FoH between children with normal HbA1c (≤ 7.5%)
56
57 and those with elevated HbA1c (>7.5%). One could conclude that FoH in both the
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64 13
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 patient and his/her caretaker is a complex concept and its impact on diabetes
1
2 management still remains unclear.
3
4
5
6 Another interesting finding of the present study was the absence of a correlation
7
8
9
between the FoH and the age of the patients, as well as the duration of diabetes. Even
10
11 though parents of younger children scored on average a little higher than parents of
12
13 adolescents, the difference was not significant. Similarly, no significant difference was
14
15
16 found in the FoH reported between the younger and older children. It could be
17
18 hypothesized that having a younger child with T1DM may exert more psychological
19
20
21 pressure on the parents due to reduced capacity of the child to manage difficult
22
23 situations related to diabetes, such as a severe hypoglycaemic episode. It could also be
24
25
26 speculated that a longer duration of diabetes may suggest familiarity with diabetes
27
28 management, hence reduced diabetes-related anxiety. However, none of the above
29
30 hypotheses were confirmed by our findings.
31
32
33
34 Furthermore, no significant differences were observed when the role of the mode of
35
36
37
treatment on parents’ and children’s FoH was assessed, although parents of children
38
39 treated via an insulin pump exhibited slightly higher HFS scores compared to those of
40
41 children on MDI. Other studies have also shown that families of insulin pump treated
42
43
44 children did not have lower FoH, although pump therapy has been reported to be
45
46 associated with lower overall diabetes-related stress in parents of paediatric patients
47
48
49 [25]. In any case, our findings should be interpreted cautiously due to the small sample
50
51 of the insulin pump treated children and adolescents.
52
53
54
55 To our surprise, although a positive relationship between severe hypoglycaemic
56
57 episodes and FoH was anticipated, experiencing more than one severe hypoglycaemic
58
59
60 episode during the previous 12 months did not have any effect on the parents’ scores
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64 14
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 of FoH. On the contrary, it did influence negatively the children’s scores for the HFS
1
2 Behaviour subscale and for the Total HFS scale. One possible explanation of this
3
4
5 finding may be that the novel advances in technology that have improved glucose
6
7 monitoring may have played a role in significantly reducing the psychological burden
8
9
10 of hypoglycaemia for the parents. Real-time continuous glucose monitoring or “flash”
11
12 monitoring provides information regarding the glucose trend and an upcoming
13
14
15 hypoglycaemia. In addition, repeated severe hypoglycaemic episodes may familiarize
16
17 children with the condition, and previous successful management may be reassuring.
18
19
20
21 With respect to moderate episodes, more than two moderate hypoglycaemic episodes
22
23 during the previous 6 months did not affect parental FoH, whereas they were associated
24
25
26 with a lower FoH in children. Mild hypoglycaemic episodes did not have an effect on
27
28 either the parental or children’s FoH. It should be noted, though, that these results
29
30 should be interpreted cautiously as there might be recall or report bias by the parents or
31
32
33 the children.
34
35
36
37
In conclusion, the present study highlights the importance of screening for FoH in
38
39 children and adolescents with T1DM and their parents, confirming literature reports of
40
41 increased psychological burden for the entire family after T1DM is diagnosed. It is
42
43
44 important to remember that patients often have limited knowledge about
45
46 hypoglycaemia beyond ‘survival skills’, which may undermine glycaemic
47
48
49 management and cause severe stress. The finding that parents reported higher levels
50
51 of FoH compared to their children underlines the significance of targeting parental fear
52
53
54 also. Increased awareness in children’s health care providers should be instituted so
55
56 that they are not only focused on the children’s glycaemic control and psychology, but
57
58
59
also on the parental emotional stress, so that appropriate psychological support can be
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64 15
65
 offered when needed. This is particularly important since this fear may be associated
1
2 with worse diabetes management and increased psychiatric morbidity in all members
3
4
5 of the family of a child with diabetes. Our findings enhance the existing knowledge on
6
7 the subject; however, it is important to note that associations between FoH and
8
9
10 demographic or disease-related parameters deserve further exploration.
11
12
13
14
15
16
17
18 Author contributions
19
20
21 Ourania Andreopoulou, Eirini Kostopoulou, Sophia Daskalaki and Bessie E Spiliotis
22
23 contributed to the conception, design and completion of the study, as well as the
24
25
26 preparation of the final manuscript considered for publication. Eirini Kostopoulou,
27
28 Eleni Kotanidou, Ourania Andreopoulou, Sophia Daskalaki, Angeliki Vakka and
29
30
31
Assimina Galli-Tsinopoulou contributed to the acquisition, analysis and interpretation
32
33 of data. Sophia Daskalaki performed the statistical analysis. Ourania Andreopoulou,
34
35 Eirini Kostopoulou and Sophia Daskalaki drafted the work. Eleni Kotanidou, Angeliki
36
37
38 Vakka, Assimina Galli-Tsinopoulou and Bessie E Spiliotis revised the work critically
39
40 for important intellectual content. All the authors gave final approval of this version to
41
42
43 be published and agree to be accountable for all aspects of the work in ensuring that
44
45 questions related to the accuracy or integrity of any part of the work are appropriately
46
47
48
investigated and resolved.
49
50
51
52 Compliance with Ethical Standards
53
54
55 Conflict of interest: The authors have no conflict of interest to disclose.
56
57 Ethical approval: The study was in accordance with the ethical standards as laid
58
59
60 down in the 1964 Declaration of Helsinki and its later amendments and it was
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64 16
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 approved by the Research Ethics Committee of the University Hospital of Patras. No
1
2 animal studies were carried out by the authors for this article.
3
4
5 Informed consent: The current research involves the participation of human subjects.
6
7 To partake in the study, the parents of the participating children and adolescents gave
8
9
10 their informed consent in a written format and children and adolescents their informed
11
12 assent, while participation was voluntary, and anonymity was assured.
13
14
15
16
17 Data Availability Statement: The data that support the findings of this study are
18
19
available from the corresponding author upon reasonable request.
20
21
22
23 References:
24
25
26 1. Kalra S, Mukherjee JJ, Venkataraman S, Bantwai G, SHaikh S, Saboo B, Das AK,
27
28 Ramachandran A (2013) Hypoglycemia: The neglected complication. Indian J
29
30
Endocrinol Metab 17:819-834. https://doi.org/10.4103/2230-8210.117219
31
32
33 2. Cryer PE (2008) The barrier of hypoglycemia in diabetes. Diabetes 57:3169–3176.
34
35 https://doi.org/10.2337/db08-1084
36
37
38 3. Gonder-Frederick LA, Vajda KA, Schmidt KM, Cox DJ, Devries JH, Erol O, Kanc
39
40 K, Schachinger H, Snoek FJ (2013) Examining the behaviour subscale of the
41
42
43 hypoglycaemia fear survey: an international study. Diabet Med 30:603–609.
44
45 https://doi.org/10.1111/dme.12129
46
47
48
4. Hendrieckx C, Halliday JA, Bowden JP, Colman PG, Cohen N, Jenkins A, Speight
49
50 J (2014) Severe hypoglycaemia and its association with psychological well-being in
51
52 Australian adults with type 1 diabetes attending specialist tertiary clinics. Diabetes Res
53
54
55 Clin Pract 103:430–436.
56
57 https://doi.org/10.1016/j.diabres.2013.12.005
58
59
60
61
62
63
64 17
65
 5. Shalitin S, Phillip M (2008) Hypoglycemia in type 1 diabetes: a still unresolved
1
2 problem in the era of insulin analogs and pump therapy. Diabetes Care 31:121-124.
3
4
5 https://doi.org/10.2337/dc08-s228
6
7 6. Clarke W, Jones T, Rewers A, Dunger D, Klingensmith GJ (2009) Assessment and
8
9
10 management of hypoglycemia in children and adolescents with diabetes. Pediatr
11
12 Diabetes 10:134–145. https://doi.org/10.1111/j.1399-5448.2009.00583.x
13
14
15 7. Johnson SR, Cooper MN, Davis EA, Jones TW (2013) Hypoglycemia, fear of
16
17 hypoglycemia and quality of life in children with type 1 diabetes and their
18
19
parents. Diabet Med 30:1126–1131. doi: 10.1111/dme.12247
20
21
22 8. Marrero DG, Guare JC, Vandagriff JL, Fineberg NS (1997) Fear of hypoglycemia in
23
24 the parents of children and adolescents with diabetes: maladaptive or healthy response?
25
26
27 Diabetes Educ 23: 281–286.
28
29 https://doi.org/ 10.1177/014572179702300306
30
31
32 9. Clark WL, Gonder-Frederick LA, Snyder AL, Cox DJ (1998) Maternal fear of
33
34 hypoglycemia in their children with insulin dependent diabetes mellitus. J Pediatr
35
36
37
Endocrinol Metab 11: 189–194. https://doi.org/10.1515/jpem.1998.11.s1.189
38
39 10. Gonder-Frederick L, Cox D, Kovatchev B, Julian D, Clarke W (1997) The
40
41 psychosocial impact of severe hypoglycemic episodes on spouses of patients with
42
43
44 IDDM. Diabetes Care 20:1–4. https://doi.org/10.2337/diacare.20.10.1543
45
46 11. Al Hayek A, A, Robert A, A, Braham R, B, Issa B, A, Al Sabaan F, S: Predictive
47
48
49 Risk Factors for Fear of Hypoglycemia and Anxiety-Related Emotional Disorders
50
51 among Adolescents with Type 1 Diabetes. Med Princ Pract 2015;24:222-230. doi:
52
53
54 10.1159/000375306
55
56
57
58
59
60
61
62
63
64 18
65
 12. Patton SR, Dolan LM, Henry R, Powers SW (2007) Parental fear of hypoglycaemia:
1
2 young children treated with continuous subcutaneous insulin infusion. Pediatr Diabetes
3
4
5 8:362-368. https://doi.org/10.1111/j.1399-5448.2007.00242.x
6
7 13. Irvine A, Cox DJ, Gonder-Frederick L (1994) The Fear of hypoglycemia
8
9
10 scale. In Handbook of psychology and diabetes: a guide to psychological measurement
11
12 and diabetes research and practice. Edited by: Bradley C. Langhorne: Hardwood
13
14
15 Academia Publishing, pp 133–158.
16
17 14. Kostopoulou E, Andreopoulou O, Daskalaki S, Kotanidou E, Vakka A, Galli-
18
19
Tsinopoulou A, Spiliotis BE, Gonder-Frederick L, Fouzas S (2023) Translation and
20
21
22 validation study of the Hypoglycemia Fear Survey (HFS) in a Greek population of
23
24 children and adolescents with Type 1 Diabetes Mellitus and their parents. Children
25
26
27 10:1458. https://doi.org/10.3390/children10091458.
28
29 15. Cox DJ, Irvine A, Gonder-Frederick L, Nowacek G, Butterfield J (1987) Fear of
30
31
32 hypoglycemia: quantification, validation, and utilization. Diabetes Care 10: 617–621.
33
34 https://doi.org/10.2337/diacare.10.5.617
35
36
37
16. Gonder-Frederick LA, Fischer CD, Ritterband LM, Cox DJ, Hou L, DasGupta AA,
38
39 Clarke WL (2006) Predictors of fear of hypoglycaemia in adolescents with type 1
40
41 diabetes and their parents. Pediatr Diabetes 7:215-222. https://doi.org/10.1111/j.1399-
42
43
44 5448.2006.00182.x.
45
46 17. Seaquist ER, Anderson J, Childs B, et al (2013) Hypoglycemia and diabetes: a
47
48
49 report of a workgroup of the American Diabetes Association and the Endocrine
50
51 Society. Diabetes Care 36:1384–1395. https://doi.org/10.2337/dc12-2480
52
53
54 18. Wild D, von Maltzahn R, Brohan E, Christensen T, Clauson P, Gonder-Frederick
55
56 L (2007) A critical review of the literature on fear of hypoglycemia in diabetes:
57
58
59
60
61
62
63
64 19
65
 implications for diabetes management and patient education. Patient Educ Couns
1
2 68:10–15. https://doi.org/10.1016/j.pec.2007.05.003
3
4
5 19. Böhme P, Bertin E, Cosson E, Chevalier N, GEODE group (2013) Fear of
6
7 hypoglycaemia in patients with type 1 diabetes: do patients and diabetologists feel the
8
9
10 same way? Diabetes Metab 39:63–70. https://doi.org/10.1016/j.diabet.2012.10.006
11
12 20. Brazeau AS, Rabasa-Lhoret R, Strychar I, Mircescu H (2008) Barriers to physical
13
14
15 activity among patients with type 1 diabetes. Diabetes Care 31:2108–
16
17 2109. https://doi.org/10.2337/dc08-0720
18
19
21. Brod M, Rana A, Barnett AH (2012) Impact of self-treated hypoglycaemia in type
20
21
22 2 diabetes: a multinational survey in patients and physicians. Curr Med Res Opin
23
24 28:1947–1958. https://doi.org/10.1185/03007995.2012.743457
25
26
27 22. Nixon R, Pickup JC (2011) Fear of hypoglycemia in type 1 diabetes managed by
28
29 continuous subcutaneous insulin infusion: is it associated with poor glycemic
30
31
32 control? Diabetes Technol Ther 13:93–98. https://doi.org/10.1089/dia.2010.0192
33
34 23. Anderbro T, Amsberg S, Adamson U, Bolinder J, Lins PE, Wredling R (2010) Fear
35
36
37
of hypoglycaemia in adults with type 1 diabetes. Diabet Med 27:1151–1158.
38
39 https://doi.org/10.1111/j.1464-5491.2010.03078.x
40
41 24. Green LB, Wysocki T, Reineck BM (1990) Fear of hypoglycemia in children and
42
43
44 adolescents with diabetes. J Pediatr Psychol 15:633–641.
45
46 25. Streisand R, Swift E, Wickmark T, Chen R, Holmes C (2005) Pediatric parenting
47
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49 stress among parents of children with type 1 diabetes: the role of self-efficacy,
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51 responsibility, and fear. J Pediatr Psychol 30:513–521.
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54 https://doi.org/10.1093/jpepsy/jsi076
55
56 Tables
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 Table 1. Sample characteristics of the studied children and adolescents (N=100):
1
2 current age, age at onset of T1DM, duration of T1DM, recent HbA1c.
3
4
5 Characteristic Min Max Mean Std Dev.
6 Current age 5.8 20.0 13.70 3.35
7 Male 6.3 20.0 13.71 3.53
8
9
Female 5.8 18.4 13.70 3.18
10 Age at onset of T1DM* 1.25 16.50 8.65 3.91
11 Male 1.25 16.50 8.71 3.73
12 Female 1.25 15.90 8.59 4.16
13
14
Time with Diabetes 0.25 16.73 5.05 4.09
15 Male 0.25 15.00 5.00 4.01
16 Female 0.25 16.73 5.11 4.23
17 Recent HbA1c** 5.0 9.4 7.27 0.98
18 Male 5.0 9.0 7.08 0.98
19
20 Female 5.4 9.4 7.49 0.95
* T1DM: ** HbA1c:
21 Type 1 diabetes mellitus, Glycosylated haemoglobin.
22
23
24
25 Table 2. Mean scores and standard deviations for HFS (Behaviour, Worry and Total
26
27
28 Scales) for the studied parents and children.
29
30 P-HFS C-HFS
31 Mean Std Dev. Mean Std Dev.
32
33
HFS Behaviour 2.14 0.56 1.80 0.74
34 HFS Worry 1.52 1.04 0.88 0.65
35 HFS Total 1.78 0.69 1.25 0.53
36
37
38
39 Table 3. Mean scores and standard deviations (in parentheses) of Behaviour, Worry
40
41 and Total HFS scales for parents and children according to patient’s age group, mode
42
43
44 of treatment, good (HbA1c ≤ 7.5 %) versus poor (HbA1C > 7%) glycaemic control.
45
46
47 P-HFS Age 6-11 (N=28) Age 12-18 (N=72)
48
49 Mean HFS Behaviour 2.19 (0.47) 2.13 (0.59)
50
51 Mean HFS Worry 1.60 (1.08) 1.48 (1.03)
52
53 Mean Total HFS 1.85 (0.71) 1.76 (0.69)
54
55
56
C-HFS Age 6-11 (N=28) Age 12-18 (N=72)
57
58 Mean HFS Behaviour 1.85 (0.64) 1.77 (0.78)
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60
61
62
63
64 21
65
 1
Mean HFS Worry 0.86 (0.71) 0.89 (0.63)
2
3 Mean Total HFS 1.26 (0.56) 1.25 (0.52)
4
5 P-HFS MDI (N=85) Pump (N=14)
6
7 Mean HFS Behaviour 2.12 (0.58) 2.26 (0.47)
8
9 Mean HFS Worry 1.52 (1.04) 1.57 (1.09)
10
11 1.78 (0.69) 1.86 (0.76)
Mean Total HFS
12
13
14 C-HFS MDI (N=85) Pump (N=14)
15
16 Mean HFS Behaviour 1.80 (0.74) 1.73 (0.72)
17
18 Mean HFS Worry 0.86 (0.63) 1.02 (0.79)
19
20 Mean Total HFS 1.24 (0.50) 1.30 (0.68)
21
22 P-HFS HbA1c ≤ 7,5 % (N=62) HbA1c > 7,5 % (N=38)
23
24
25 Mean HFS Behaviour 2.11 (0.60) 2.20 (0.48)
26
27 Mean HFS Worry 1.34* (0.95) 1.81* (1.11)
28
29 Mean Total HFS 1.66* (0.66) 1.98* (0.70)
30
31 C-HFS HbA1c ≤ 7.5 % (N=62) HbA1c > 7.5 % (N=38)
32
33 Mean HFS Behaviour 1.90 (0.68) 1.62 (0.79)
34
35
36
Mean HFS Worry 0.86 (0.65) 0.93 (0.65)
37
38 Mean Total HFS 1.28 (0.52) 1.20 (0.54)
39
40
*Significant difference at the 0.05 level (2-tailed),
41
42 **Significant difference at the 0.01 level (2-tailed).
43
44
45
46 Table 4. Mean scores and standard deviations (in parentheses) of Behaviour, Worry
47
48
49 and Total HFS scales for parents and children according to the frequency of severe,
50
51 moderate and mild hypoglycaemic episodes. SH: severe hypoglycaemic episode, MeH:
52
53
54 moderate hypoglycaemic episode, MiH: mild hypoglycaemic episode.
55
56
57
58 P-HFS SH ≤ 1 (N=83) SH > 1 (N=12)
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64 22
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 1
Mean HFS Behaviour 2.12 (0.54) 2.10 (0.54)
2
3 Mean HFS Worry 1.54 (1.01) 1.30 (1.14)
4
5 Mean Total HFS 1.79 (0.67) 1.64 (0.80)
6
7 C-HFS SH ≤ 1 (N=76) SH > 1 (N=15)
8
9 Mean HFS Behaviour 1.89* (0.70) 1.17* (0.70)
10
11 0.92 (0.68) 0.77 (0.62)
Mean HFS Worry
12
13
14 Mean Total HFS 1.31* (0.51) 0.94* (0.60)
15
16 P-HFS MeH ≤ 2 (N=60) MeH > 2 (N=34)
17
18 Mean HFS Behaviour 2.16 (0.59) 2.02 (0.45)
19
20 Mean HFS Worry 1.47 (0.93) 1.55 (1.19)
21
22 Mean Total HFS 1.76 (0.63) 1.76 (0.78)
23
24
25 C-HFS MeH ≤ 2 (N=56) MeH > 2 (N=35)
26
27 Mean HFS Behaviour 1.97** (0.73) 1.47** (0.67)
28
29 Mean HFS Worry 0.96 (0.72) 0.79 (0.58)
30
31 Mean Total HFS 1.36** (0.55) 1.07** (0.48)
32
33 P-HFS MiH ≤ 3 (N=48) MiH > 3 (N=48)
34
35
36
Mean HFS Behaviour 2.04 (0.58) 2.22 (0.49)
37
38 Mean HFS Worry 1.36 (1.02) 1.74 (1.04)
39
40 Mean Total HFS 1.65 (0.70) 1.95 (0.68)
41
42 C-HFS MiH ≤ 3 (N=43) MiH > 3 (N=49)
43
44 Mean HFS Behaviour 1.72 (0.79) 1.81 (0.71)
45
46
47
Mean HFS Worry 0.93 (0.77) 0.86 (0.57)
48
49 Mean Total HFS 1.25 (0.56) 1.24 (0.53)
50 *Significant difference at the 0.05 level (2-tailed),
51 **Significant difference at the 0.01 level (2-tailed).
52
53
54
55
56
Figure Legends
57
58 Fig. 1 Mean scores of different items of the P-HFS and C-HFS scales.
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64 23
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 1
2 Supplementary File 1 Children’s and parents’ responses regarding the frequency of
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5 severe, moderate and mild hypoglycaemic episodes during the previous year, previous
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7 6 months and previous month, respectively.
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Table 1 Click here to access/download;Table;Table 1 revised.docx

Characteristic Min Max Mean Std Dev.

Current age 5.8 20.0 13.70 3.35
Male 6.3 20.0 13.71 3.53
Female 5.8 18.4 13.70 3.18
Age at onset of T1DM* 1.25 16.50 8.65 3.91
Male 1.25 16.50 8.71 3.73
Female 1.25 15.90 8.59 4.16
Duration of T1DM 0.25 16.73 5.05 4.09
Male 0.25 15.00 5.00 4.01
Female 0.25 16.73 5.11 4.23
Recent HbA1c** 5.0 9.4 7.27 0.98
Male 5.0 9.0 7.08 0.98
Female 5.4 9.4 7.49 0.95
* T1DM: ** HbA1c:
Type 1 diabetes mellitus, Glycosylated haemoglobin.
Table 2 Click here to access/download;Table;Table 2 revised.docx

P-HFS C-HFS
Mean Std Dev. Mean Std Dev.
HFS Behaviour 2.14 0.56 1.80 0.74
HFS Worry 1.52 1.04 0.88 0.65
HFS Total 1.78 0.69 1.25 0.53
Table 3 Click here to access/download;Table;Table 3.docx

Table 3.

P-HFS Age 6-11 (N=28) Age 12-18 (N=72)

Mean HFS Behaviour 2.19 (0.47) 2.13 (0.59)

Mean HFS Worry 1.60 (1.08) 1.48 (1.03)

Mean Total HFS 1.85 (0.71) 1.76 (0.69)

C-HFS Age 6-11 (N=28) Age 12-18 (N=72)

Mean HFS Behaviour 1.85 (0.64) 1.77 (0.78)

Mean HFS Worry 0.86 (0.71) 0.89 (0.63)

Mean Total HFS 1.26 (0.56) 1.25 (0.52)

P-HFS MDI (N=85) Pump (N=14)

Mean HFS Behaviour 2.12 (0.58) 2.26 (0.47)

Mean HFS Worry 1.52 (1.04) 1.57 (1.09)

Mean Total HFS 1.78 (0.69) 1.86 (0.76)

C-HFS MDI (N=85) Pump (N=14)

Mean HFS Behaviour 1.80 (0.74) 1.73 (0.72)

Mean HFS Worry 0.86 (0.63) 1.02 (0.79)

Mean Total HFS 1.24 (0.50) 1.30 (0.68)

P-HFS HbA1c ≤ 7,5 % (N=62) HbA1c > 7,5 % (N=38)

Mean HFS Behaviour 2.11 (0.60) 2.20 (0.48)

Mean HFS Worry 1.34* (0.95) 1.81* (1.11)

Mean Total HFS 1.66* (0.66) 1.98* (0.70)

C-HFS HbA1c ≤ 7.5 % (N=62) HbA1c > 7.5 % (N=38)

Mean HFS Behaviour 1.90 (0.68) 1.62 (0.79)

Mean HFS Worry 0.86 (0.65) 0.93 (0.65)

Mean Total HFS 1.28 (0.52) 1.20 (0.54)

*Significant difference at the 0.05 level (2-tailed),

**Significant difference at the 0.01 level (2-tailed).
Table 4 Click here to access/download;Table;Table 4.docx

P-HFS SH ≤ 1 (N=83) SH > 1 (N=12)

Mean HFS Behaviour 2.12 (0.54) 2.10 (0.54)

Mean HFS Worry 1.54 (1.01) 1.30 (1.14)

Mean Total HFS 1.79 (0.67) 1.64 (0.80)

C-HFS SH ≤ 1 (N=76) SH > 1 (N=15)

Mean HFS Behaviour 1.89* (0.70) 1.17* (0.70)

Mean HFS Worry 0.92 (0.68) 0.77 (0.62)

Mean Total HFS 1.31* (0.51) 0.94* (0.60)

P-HFS MeH ≤ 2 (N=60) MeH > 2 (N=34)

Mean HFS Behaviour 2.16 (0.59) 2.02 (0.45)

Mean HFS Worry 1.47 (0.93) 1.55 (1.19)

Mean Total HFS 1.76 (0.63) 1.76 (0.78)

C-HFS MeH ≤ 2 (N=56) MeH > 2 (N=35)

Mean HFS Behaviour 1.97** (0.73) 1.47** (0.67)

Mean HFS Worry 0.96 (0.72) 0.79 (0.58)

Mean Total HFS 1.36** (0.55) 1.07** (0.48)

P-HFS MiH ≤ 3 (N=48) MiH > 3 (N=48)

Mean HFS Behaviour 2.04 (0.58) 2.22 (0.49)

Mean HFS Worry 1.36 (1.02) 1.74 (1.04)

Mean Total HFS 1.65 (0.70) 1.95 (0.68)

C-HFS MiH ≤ 3 (N=43) MiH > 3 (N=49)

Mean HFS Behaviour 1.72 (0.79) 1.81 (0.71)

Mean HFS Worry 0.93 (0.77) 0.86 (0.57)

Mean Total HFS 1.25 (0.56) 1.24 (0.53)

SH: Severe hypoglycaemic episodes, MeH: moderate hypoglycaemic episodes, MiH: mild hypoglycaemic episodes
*Significant difference at the 0.05 level (2-tailed),
**Significant difference at the 0.01 level (2-tailed).
Figure 1 Click here to access/download;Figure;Fig. 1.jpg
Supplementary Material

Click here to access/download

Supplementary Material
Supplementary file 1.docx